The cone photoreceptors and visual pigments of chameleons

Visual pigments, oil droplets and photoreceptor types in the retinas of four species of true chameleons have been examined by microspectrophotometry. The species occupy different photic environments: two species of Chamaeleo are from Madagascar and two species of Furcifer are from Africa and the Arabian Peninsula. In addition to double cones, four spectrally distinct classes of single cone were identified. No rod photoreceptors were observed. The visual pigments appear to be mixtures of rhodopsins and porphyropsins. Double cones contained a pale oil droplet in the principle member and both outer segments contained a long-wave-sensitive visual pigment with a spectral maximum between about 555 nm and 610 nm, depending on the rhodopsin/porphyropsin mixture. Long-wave-sensitive single cones contained a visual pigment spectrally identical to the double cones, but combined with a yellow oil droplet. The other three classes of single cone contained visual pigments with maxima at about 480–505, 440–450 and 375–385 nm, combined with yellow, clear and transparent oil droplets respectively. The latter two classes were sparsely distributed. The transmission of the lens and cornea of C. dilepis was measured and found to be transparent throughout the visible and near ultraviolet, with a cut off at about 350 nm.     

Visual pigments, cone oil droplets and ocular media in four species of estrildid finch

A microspectrophotometric study was conducted on the retinal photoreceptors of four species of bird: cut-throat finches (Amadina fasciata), gouldian finches (Erythrura gouldiae), white-headed munias (Lonchura maja) and plum-headed finches (Neochmia modesta). Spectral characteristics of the photoreceptors in all four species were very similar. Rods contained a medium-wavelength-sensitive visual pigment with a wavelength of maximum absorbance at 502-504 nm. Four spectrally distinct types of single cone contained a visual pigment with wavelength of maximum absorbance at either 370-373 nm (ultraviolet-sensitive), 440-447 nm (short-wavelength-sensitive); 500 nm (medium-wavelength-sensitive) or 562-565 nm (long-wavelength-sensitive). Oil droplets in the ultraviolet-sensitive single cones showed no detectable absorption between 330 nm and 800 nm. Oil droplets in the short-, medium-, and long-wavelength-sensitive single cones had cut-off wavelengths at 415-423 nm, 510-520 nm and 567-575 nm, respectively. Double cones contained the visual pigment with wavelength of maximum absorbance at 562-565 nm observed in long-wavelength-sensitive single cones. Only the principal member of the double cone pair contained an oil droplet (P-type, cut-off wavelength at 414-489 nm depending on species and retinal location). Spectral transmittance of the intact ocular media of each species was measured along the optic axis. Wavelengths of 0.5 transmittance for all species were very similar (316-318 nm).     

Tetrachromatic colour vision in the duck (Anas platyrhynchos L.):microspectrophotometry of visual pigments and oil droplets

Summary Microspectrophotometric examination of the visual receptors of the duck,Anas platyrhynchos, revealed four types of single cone containing visual pigments absorbing maximally at about 420 nm, 452 nm, 502 nm and 570 nm. A single population of double cones contained the P570 in both members. Rods absorbed maximally at 505 nm.Within the single cones, three types of oil droplet, acting as cut-off filters, were identified by the wavelength at which 50% transmission occurred, approximately 580, 515 and 450 nm. A further droplet, transparent throughout the visible spectrum, was also found in a small population of single cones. A fifth droplet type with a variable cutoff between 475–500 nm was located in the principal member of the double cones.The optical density of the anterior half of the eye, established by spectrophotometry, was used, in conjunction with the visual pigment and oil droplet combinations found within intact cones, to estimate the relative spectral sensitivities of the major cone types within the retina.     

Spectral sensitivities including the ultraviolet of the passeriform bird Leiothrix lutea

Spectral sensitivity functions of a passeriform bird, the Red-billed Leiothrix Leiothrix lutea (Timalidae) were determined in a behavioural test under different background illuminations.

Visual pigments and oil droplets in the penguin,Spheniscus humboldti

Summary The photoreceptors of the penguin,Spheniscus humboldti, were examined using a microspectrophotometer. The cones could be divided into three classes based on their visual pigment absorbance spectra [max 403, 450 and 543 nm (Fig. 1)], and into five classes based on their visual pigment-oil droplet combination (Fig. 4). Oil droplets were of three types (Fig. 2). The rods contained a rhodopsin with max at 504 nm. No double cones were observed. The penguin should be capable of good wavelength discrimination in the blue-green region of the spectrum but with poor discrimination at longer wavelengths. It is concluded that the spectral properties of the cone types indicate that the photopic vision ofS. humboldti is adapted to the spectral qualities of its aquatic environment.     

Photoreceptors and photopigments in a subterranean rodent,the pocket gopher (<Emphasis Type="Italic">Thomomys bottae</Emphasis>)

Pocket gophers (Thomomys bottae) are rodents that spend much of their lives in near-lightless subterranean burrows. The visual adaptations associated with this extreme environment were investigated by making anatomical observations of retinal organization and by recording retinal responses to photic stimulation. The size of the eye is within the normal range for rodents, the lens transmits light well down into the ultraviolet, and the retina conforms to the normal mammalian plan. Electroretinogram recording revealed the presence of three types of photopigments, a rod pigment with a spectral peak of about 495 nm and two types of cone pigment with respective peak values of about 367 nm (UV) and 505 nm (medium-wavelength sensitive). Both in terms of responsivity to lights varying in temporal frequency and in response recovery following intense light adaptation, the cone responses of the pocket gopher are similar to those of other rodents. Labeling experiments indicate an abundance of cones that reach densities in excess of 30,000 mm^–2. Cones containing UV opsin are found throughout the retina, but those containing medium-wavelength sensitive opsin are mostly restricted to the dorsal retina where coexpression of the two photopigments is apparently the rule. Rod densities are lower than those typical for nocturnal mammals.     

Das UV-Sehen der V?gel: Neue Ergebnisse über den spektralen Sehbereich der V?gel

Zusammenfassung Ergebnisse aus einem mikrospektrophotometrischen sowie einem verhaltensphysiologischen Versuchsansatzes zeigen, daß der SonnenvogelLeiothrix lutea einen eigenständigen UV-Zapfentyp besitzt und eine sehr hohe Empfindlichkeit im UV-Teil des Spektrums aufweist. Diese Befunde werden mit den Ergebnissen anderer Autoren verglichen, die zeigen, daß eine Vielzahl von Vogelarten UV-empfindlich ist (entweder mit einem UV-Rezeptor oder eingeschränkt mit einem Violett-Rezeptor). Diese UV-Empfindlichkeit könnten Vögel nützen zur Orientierung am Polarisationsmuster der Sonne, zur Art-und/oder Partnererkennung, bzw. zur Nahrungssuche.

---

UV vision in birds: A summary of latest results concerning the extended spectral range of birds

The results of a microspectrophotometric and a behavioural test present evidence that the passeriform birdLeiothrix lutea (Timaliidae) possesses a genuine UV cone type and is highly sensitive in the UV part of the spectrum. Those data are in accordance with results of other tests indicating that a majority of bird species is UV sensitive (either by a UV cone type or somewhat limited by a violet cone typ). Possible use of this extended sensitivity like orientation according to the polarisation pattern of the sky, species and/or mate recognition and food detection are discussed.

     

Color vision of the budgerigar (<Emphasis Type="Italic">Melopsittacus undulatus</Emphasis>): hue matches,tetrachromacy, and intensity discrimination

Budgerigars, Melopsittacus undulatus, were trained to discriminate monochromatic lights from mixtures of two comparison lights. The addition of small amounts of UV (365 nm) to blue or yellow lights dramatically changed the color for the birds. Hue matches showed the birds to be dichromatic both at long wavelengths (only P565 and P508 active) and at short wavelengths (only P370 and P445 active because of screening of P508 and P565 by cone oil droplets). In mid-spectrum (only P445 and P508 active), a hue match was achieved, but the results were more complicated because two opponent neural processes were activated. All observed hue matches were in quantitative agreement with calculations of relative quantum catch in the pairs of participating single cones and point to the presence of a minimum of three opponent neural processes. For the hue matches at mid- and short wavelengths, the calculations also predict peak values of absorbance of the cone oil droplets associated with P508 and P445. Relative intensity of the training light affected difficult matches at long but not short wavelengths, likely due to achromatic signals from the double cones. With suitable training, birds could make intensity discriminations at short wavelengths, where the double cones have diminished sensitivity.     

Four spectral classes of cone in the retinas of birds

Summary The spectral sensitivity of 15 species of birds has been measured by recording transretinal voltages from opened eyecups. With suitable combinations of colored adapting lights, we find that a variety of passerines have four peaks of photopic sensitivity, with maxima at 370, 450, 480, and 570 nm. Additional sensitivity maxima at 510 nm are found in some species. The spectral sensitivity functions are not altered by bathing the retinas in 50 mM sodium aspartate, suggesting that they reflect the properties of cones and do not result from inhibitory interactions between retinal interneurons.Comparison of the results with a general mathematical model that describes spectral sensitivity functions recorded extracellularly from populations of receptors in different states of adaptation (Goldsmith 1986) shows that the retinal spectral sensitivity functions are consistent with the presence of (at least) four types of cone, but indicate as well that many of the cones that are maximally sensitive in the blue and violet likely contain oil droplets that attenuate the deep violet and near uv.     

Optimal mechanisms for finding and selecting mates: how threespine stickleback (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>) should encode male throat colors

Male threespine stickleback (Gasterosteus aculeatus) use nuptial colors to attract mates and intimidate rivals. We quantified stickleback color and environmental lighting using methods independent of human perception to evaluate the information transmitted by male signals in a habitat where these signals are displayed. We also developed models of chromatic processing based on four cone photopigments (peak absorptions at 360, 445, 530, and 605 nm) characterized microspectrophotometrically in G. aculeatus and three other stickleback species. We show that a simple opponent mechanism receiving equally weighted inputs from cones with peak absorptions at 445 nm and 605 nm efficiently encodes variation in male throat colors. An orthogonal opponent mechanism—the difference between outputs of 530-nm cones and mean of outputs of 445- and 605-nm cones—produces a neural signal that could be used for species recognition and would be largely insensitive to variation in male throat color. We also show that threespine stickleback throats/photopigments are optimized for this coding scheme. These and other findings lead to testable hypotheses about the spectral processing mechanisms present in the threespine stickleback visual systems and the evolutionary interactions that have shaped this signal/receiver system.Abbreviations LWS long-wave sensitive - MWS middle-wave sensitive - SWS short-wave sensitive - UVS ultra-violet sensitive     

Immunohistochemical localization of iodopsin in the retina of the chicken and Japanese quail

Summary Localization of iodopsin in the retina of the chicken and Japanese quail was investigated immunohistochemically with the use of monoclonal antibodies (R1-R4) highly specific for R-photopsin (protein moiety of iodopsin). In paraffin sections of the retina, the outer segments of double cones (principal and accessory cones) and of one particular type of single cones were labeled with the antibodies. In addition, reticular cytoplasmic structures, probably representing the Golgi apparatus in a position close to the vitreous pole of the paraboloid and to the outer limiting membrane were intensely stained in the cone cells bearing an immunoreactive outer segment. In whole-mount preparations, 5 types of cone cells were identified according to the color of oil droplets, i.e., red, yellow, pale-green (principal member of double cones), pale-blue and clear, in addition to a sixth type devoid of an oil droplet (accessory member of double cones). The immunohistochemical analysis of the preparations revealed that R-photopsin (suggesting the presence of iodopsin) is localized in the outer segments of both the principal and accessory members of double cones, and the population of single cones displaying a red oil droplet. Other cones endowed with a yellow, blue or clear oil droplet were not labeled with the antibodies used. Similar results were obtained in the retina of the Japanese quail.     

The photoreceptors and visual pigments of the garter snake (Thamnophis sirtalis): a microspectrophotometric, scanning electron microscopic and immunocytochemical study

Scanning electron microscopy, immunocytochemistry, and single cell microspectrophotometry were employed to characterize the photoreceptors and visual pigments in the retina of the garter snake, Thamnophis sirtalis. The photoreceptor population was found to be comprised entirely of cones, of which four distinct types were identified. About 45.5% of the photoreceptors are double cones consisting of a large principal member joined near the outer segment with a much smaller accessory member. About 40% of the photoreceptors are large single cones, and about 14.5% are small single cones forming two subtypes. The outer segments of the large single cones and both the principal and accessory members of the doubles contain the same visual pigment, one with peak absorbance near 554 nm. The small single cones contain either a visual pigment with peak absorbance near 482 nm or one with peak absorbance near 360 nm. Two classes of small single cones could be distinguished also by immunocytochemistry and scanning electron microscopy. The small single cones with the 360-nm pigment provide the garter snake with selective sensitivity to light in the near ultraviolet region of the spectrum. This ultraviolet sensitivity might be important in localization of pheromone trails. Accepted: 10 March 1997     

Localization of visual pigment antigens to photoreceptor cells with different oil droplets in the chicken retina

Frozen semithin sections and unembedded retinal pieces were investigated by immunocytochemistry using two antibodies produced against visual pigments in our laboratory. One was a polyclonal serum (AO) raised against bovine rhodopsin, while the other one was a monoclonal antibody (COS-1) produced against an epitope present in a cone visual pigment. AO stained, as expected, rod outer segments; in addition it also recognized a single cone characterized by a deep yellow oil droplet as well as another single cone with a yellowish green oil droplet. In contrast, COS-1 labelled both members of the double cones; the principal member having a yellowish-green oil droplet and the accessory member. COS-1 also stained a single cone type exhibiting a large red oil droplet.     

Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors

Birds have four spectrally distinct types of single cones that they use for colour vision. It is often desirable to be able to model the spectral sensitivities of the different cone types, which vary considerably between species. However, although there are several mathematical models available for describing the spectral absorption of visual pigments, there is no model describing the spectral absorption of the coloured oil droplets found in three of the four single cone types. In this paper, we describe such a model and illustrate its use in estimating the spectral sensitivities of single cones. Furthermore, we show that the spectral locations of the wavelengths of maximum absorbance (_max) of the short- (SWS), medium- (MWS) and long- (LWS) wavelength-sensitive visual pigments and the cut-off wavelengths (_cut) of their respective C-, Y- and R-type oil droplets can be predicted from the _max of the ultraviolet- (UVS)/violet- (VS) sensitive visual pigment.     

Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.)

The spectral absorption characteristics of the retinal photoreceptors of the blue tit (Parus caeruleus) and blackbird (Turdus merula) were investigated using microspectrophotometry. The retinae of both species contained rods, double cones and four spectrally distinct types of single cone. Whilst the visual pigments and cone oil droplets in the other receptor types are very similar in both species, the wavelength of maximum sensitivity (λ_max) of long-wavelength-sensitive single and double cone visual pigment occurs at a shorter wavelength (557 nm) in the blackbird than in the blue tit (563 nm). Oil droplets located in the long-wavelength-sensitivesingle cones of both species cut off wavelengths below 570–573 nm, theoretically shifting cone peak spectral sensitivity some 40 nm towards the long-wavelength end of the spectrum. This raises the possibility that the precise λ_max of the long-wavelength-sensitive visual pigment is optimised for the visual function of the double cones. The distribution of cone photoreceptors across the retina, determined using conventional light and fluorescence microscopy, also varies between the two species and may reflect differences in their visual ecology. Accepted: 8 January 2000     

Spectral sensitivity of ground squirrel cones measured with ERG flicker photometry

Summary Ground squirrels have dichromatic color vision. The spectral sensitivities of the two classes of cones found in the retinas of two species of ground squirrel were measured using ERG flicker photometry. The spectral sensitivity curves for these cone classes were closely fit by curves from wavelength-dependent visual pigment nomograms. One cone type had an average peak sensitivity of 518.9 nm (California ground squirrels,Spermophilus beecheyi) or 517.0 nm (thirteen-lined ground squirrels,Spermophilus tridecemlineatus). The second type of cone found in these ground squirrels had an average peak sensitivity of 436.7 nm. An examination of the variation in spectral sensitivity among individual animals suggests that the sensitivity peaks for the middle-wavelength cone cover a range of not greater than 4 nm.     

Retinal ellipsosomes: morphology,development, identification,and comparison with oil droplets

We report some unique features of retinal cone ellipsosomes in mountain-stream teleosts. They have also been compared with oil droplets occurring predominantly in many reptilian and avian retinas. Ontogenetically, ellipsosome differentiation from ellipsoidal mitochondria occurs with advance eye growth (diameter>1 mm). In juvenile loaches, they arise almost simultaneously in the dorsal and ventral retina, whereas in cyprinids, they appear first dorsally in bottom-dwelling early juveniles (approximate age 3–4 months), and then in the ventral retina in migratory late juveniles (eye diameter>4 mm, approximate age 2 years). The significance of the pattern of ontogeny of ellipsosomes in these stream fishes is discussed in relation to their utilization of a complex habitat during life. All adult cones possess conspicuous ellipsosomes. Histochemically, they react strongly with phosphotungstic-acid hematoxylin, a dye specific for proteins, whereas oil droplets refuse to do so (studied in turtle and pigeon). This reflects a major chemical difference between the two types of globules. Since ellipsosomes are present in the double cone accessory unit (which in higher vertebrates lacks an oil droplet) and since they appear late ontogenetically during advanced eye growth, they cannot be related to oil droplets, which have an embryonic developmental program.     

Cone photopigments in nocturnal and diurnal procyonids

Summary Procyonids are small, New World carnivores distributed among some 6 genera. Electroretinogram (ERG) flicker photometry was used to measure the spectra of the cone photopigments for members of two nocturnal species, the raccoon (Procyon lotor) and the kinkajou (Potos flavus), and a diurnal species, the coati (Nasua nasua). Each of the 3 has a class of cone photopigment with maximum sensitivity in the middle to long wavelengths. The spectral positioning of this cone is different for the three. Whereas the raccoon and kinkajou are monochromatic, the diurnal coati is a dichromat having an additional class of cone photopigment with peak sensitivity close to 433 nm.Abbreviations ERG electroretinogram - SWS short wavelength sensitive     

Changes in the spectral absorption of cone visual pigments during the settlement of the goatfish Upeneus tragula: the loss of red sensitivity as a benthic existence begins

The goatfish Upeneus tragula undergoes an abrupt metamorphosis at settlement when the pelagic larvae begin a reef-associated benthic mode of life. A microspectrophotometric investigation of the retinal visual pigments was carried out on fish prior to, during, and following settlement. It was found that the visual pigment in the long wavelength-absorbing member of the double cones in the dorsal retina changed rapidly from a rhodopsin with a wavelength of maximum absorption (max) of 580 nm to that of 530 nm. The second member of the double cones always had a rhodopsin with the max absorbing at shorter wavelengths. Prior to settlement the average for this class of cones was 487 nm whereas during and immediately following the settlement period the max recorded from individual outer segments was found to vary between 480 nm and 520 nm, with two possible classes of cone absorbance emerging within this range. These two classes of absorbance had average max values of 487 and 515 nm. The average max of the paired cone classes in one larger wild-settled fish were found to be at 506 nm and 530 nm. No change was detected in the max of the single cones or the rods which were always found to have a max of about 400 nm and 498 nm respectively. The loss of the redabsorbing pigment occurred over the same time scale as the metamorphosis of morphological features associated with the settlement process. It is thought that the loss of this visual pigment is associated with the change in light environment of the fishes as they leave the surface waters to begin a benthic mode of life in deeper water.Abbreviations AIMS Australian Institute of Marine Science - ANOVA Analysis of variance - IR infra-red - max wavelength of maximum absorption - MSP microspectrophotometer - NA numerical aperture - SL standard length     

The all-cone retina of the garter snake: spectral mechanisms and photopigment

Summary The retina of the garter snake contains 3 morphologically distinct classes of cone photoreceptor. The spectral mechanisms in the retinas of garter snakes (Thamnophis sirtalis and T. marcianus) were studied by recording a retinal gross potential, the electroretinogram, using a flicker photometric procedure. Spectral sensitivity functions recorded with stimuli presented at high temporal frequency (62.5 Hz) are broadly peaked in the region of 550–570 nm. These functions remain spectrally invariant (a) in the face of significant changes in stimulus pulse rate (8–62.5 Hz), (b) whether the eye is light or dark adapted, and (c) under conditions of intense chromatic adaptation. It is concluded that the garter snake has only a single class of cone pigment. The results from a curve fitting analysis suggests that this pigment has peak absorbance at about 556 nm.